7.4 The dikaryon

In the Basidiomycota the heterokaryon is highly specialised, being made up of
cells that each contains nuclei from two compatible mating types within a common
cytoplasm; this is called a dikaryon. A similar arrangement exists in the
ascogenous hyphae of Ascomycota, but in many Basidiomycota the
dikaryotic condition is purposefully perpetuated by a special kind of hyphal
growth (Fig. 6) so that the dikaryotic mycelium can grow indeterminately like
any other mycelium. Under normal circumstances only dikaryotic mycelium forms
fruit bodies.

The dikaryotic state is maintained by a specialised cell biology: the nuclei
divide together (= conjugate mitosis) and at the same time a ‘clamp
connection’ grows out as a backward projecting branch which loops
backwards and then fuses with the parent hypha. One of the nuclei completes its
mitosis in the clamp connection, the other nucleus stays in the main body of the
hypha. This separation means that two normal dolipore septa can be formed
between daughters of the two mitotically-dividing nuclei and both terminal and
subterminal cells (that is, the two daughter compartments) each contain two
nuclei of opposite mating type; one nucleus of the subterminal cell being
delivered to it through the clamp connection (Fig. 6B). The regularity of this
process results in every cell of the dikaryon containing two sets of homologous
chromosomes: that is, the dikaryon is a functional diploid.

This is an important point. The so-called ‘higher organisms’ (plants and
animals) are diploid but most true fungi are haploid, and this has genetic and
evolutionary consequences. However the haploid Basidiomycota have developed
functionally diploid cells by extending the vegetative life of dikaryotic
heterokaryons and in so doing they have gained the genetic (and evolutionary)
advantages of diploid organisms, whilst remaining haploid. Like the diploid, a
dikaryotic cell also has two sets of homologous chromosomes, even though each
set is located in a separate nucleus. Together, the two nuclei control and
regulate the activities of a specific volume of cytoplasm. Complex cellular
events have been evolved by Basidiomycota to establish and maintain the
dikaryotic condition. These include different mating types and vegetative
compatibility systems, elaborate dolipore septa, and an elaborate cytokinesis
mechanism in which a backwardly directed hyphal branch enables a daughter
nucleus to leapfrog a septum and maintain the dikaryotic condition in each
daughter cell of the mitosis (Fig. 6). No wonder Basidiomycota are considered
the most advanced group of fungi.

Fig. 6. The dikaryon: a specialised binucleate
heterokaryon. The dikaryotic state is maintained by the clamp connection: a
backward-projecting hyphal branch which fuses with its parent hypha to
deliver one of the nuclei and ensure that each compartment contains two
nuclei of opposite mating type separated by a dolipore septum. Each hyphal
compartment therefore contains two sets of homologous chromosomes and is a
functional diploid.

Clamp connections are required to maintain the dikaryon because the dolipore
septum controls organelle migration and normally hinders proper nuclear
distribution. Clamp connections may not be necessary if the hypha is so wide
that the conjugate mitoses can take place without hindrance, so some vegetative
dikaryons may not form clamp connections. For most of the Basidiomycota, only
the dikaryotic mycelium can differentiate into a fruit body, but many fruit
bodies contain specialised tissues in which the dikaryotic condition breaks
down. For example, many cells in the stem of the Ink cap mushroom fruit body of
Coprinopsis are enormously enlarged and are multinucleate, whereas cells
elsewhere in the same fruit are regularly dikaryotic. Similarly, not all
basidiomycete mycelia are dikaryotic; some are multinucleate, and it is curious
that more fungi have not become true diploids. Perhaps the more flexible
heterokaryotic condition offers greater advantages than we suspect.

Dikaryon formation occurs via the activities of cell type-specific
homeodomain transcription factors (the mating type factors), which form
regulatory complexes to establish the dikaryotic state. Many years of
classical genetic studies with Coprinopsis and Schizophyllum
mushrooms created the foundation of our understanding of how the mating type
factors work. Basidiomycota includes many pathogenic fungi too, including
the corn (smut) pathogen Ustilago maydis and the globally
distributed human pathogenic Cryptococcus neoformans, a leading
cause of fungal meningitis. These two have featured in more recent molecular
studies that have revealed novel mechanisms of regulation that function
downstream of classic homeodomain complexes to ensure that dikaryons are
established and propagated (Kruzel & Hull, 2010). For example, in
Ustilago maydis, dikaryon formation is controlled by a DNA damage
response cascade that includes two conserved DNA-damage checkpoint kinases,
called Chk1 and Atr1 (Pérez-Martín & de Sena-Tomás, 2011).